Estrogen Selectively Increases Tryptophan Hydroxylase-2 mRNA Expression in Distinct Subregions of Rat Midbrain Raphe Nucleus: Association between Gene Expression and Anxiety Behavior in the Open Field

Biological Psychiatry

Volumn 60, Issue 3, 2006, Pages 288-295

  Hiroi, Ryoko ^a,b   McDevitt, Ross A ^a,b   Neumaier, John F ^b  

^a UNIVERSITY OF WASHINGTON   (United States)

^b UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

Author keywords

dorsal raphe; median raphe; Ovarian hormones; progesterone; serotonin; TPH2

Indexed keywords

ESTROGEN; MESSENGER RNA; PLACEBO; PROGESTERONE; TRYPTOPHAN HYDROXYLASE;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANXIETY; ARTICLE; BRAIN REGION; CONTROLLED STUDY; ESTROGEN ACTIVITY; FEMALE; GENE EXPRESSION; GENE EXPRESSION REGULATION; MESENCEPHALON; NONHUMAN; OPEN FIELD BEHAVIOR; OPEN FIELD TEST; OVARIECTOMY; PRIORITY JOURNAL; RAPHE NUCLEUS; RAT;

ANIMALS; ANXIETY; BEHAVIOR, ANIMAL; DENSITOMETRY; ESTROGENS; FEMALE; GENE EXPRESSION; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; OVARIECTOMY; PROGESTERONE; RAPHE NUCLEI; RATS; RATS, SPRAGUE-DAWLEY; RNA, MESSENGER; SPATIAL BEHAVIOR; TRYPTOPHAN HYDROXYLASE;

EID: 33746257117     PISSN: 00063223     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.biopsych.2005.10.019     Document Type: Article

References (80)

1. Abrams J.K., Johnson P.L., Hollis J.H., and Lowry C.A. Anatomic and functional topography of the dorsal raphe nucleus. Ann N Y Acad Sci 1018 (2004) 46-57
2. Adell A., Casanovas J.M., and Artigas F. Comparative study in the rat of the actions of different types of stress on the release of 5-HT in raphe nuclei and forebrain areas. Neuropharmacology 36 (1997) 735-741
3. Alves S.E., Weiland N.G., Hayashi S., and McEwen B.S. Immunocytochemical localization of nuclear estrogen receptors and progestin receptors within the rat dorsal raphe nucleus. J Comp Neurol 391 (1998) 322-334
4. Arpels J.C. The female brain hypoestrogenic continuum from the premenstrual syndrome to menopause. A hypothesis and review of supporting data. J Reprod Med 41 (1996) 633-639
5. Bagdy G., Graf M., Anheuer Z.E., Modos E.A., and Kantor S. Anxiety-like effects induced by acute fluoxetine, sertraline or m-CPP treatment are reversed by pretreatment with the 5-HT2C receptor antagonist SB-242084 but not the 5-HT1A receptor antagonist WAY-100635. Int J Neuropsychopharmacol 4 (2001) 399-408
6. Best N.R., Rees M.P., Barlow D.H., and Cowen P.J. Effect of estradiol implant on noradrenergic function and mood in menopausal subjects. Psychoneuroendocrinology 17 (1992) 87-93
7. Bethea C.L., Mirkes S.J., Shively C.A., and Adams M.R. Steroid regulation of tryptophan hydroxylase protein in the dorsal raphe of macaques. Biol Psychiatry 47 (2000) 562-576
8. Boldrini M., Underwood M.D., Mann J.J., and Arango V. More tryptophan hydroxylase in the brainstem dorsal raphe nucleus in depressed suicides. Brain Res 1041 (2005) 19-28
9. Boyer W.F., and Feighner J.P. An overview of paroxetine. J Clin Psychiatry 53 Suppl (1992) 3-6
10. Bridges R.S. A quantitative analysis of the roles of dosage, sequence, and duration of estradiol and progesterone exposure in the regulation of maternal behavior in the rat. Endocrinology 114 (1984) 930-940
11. Burghardt N.S., Sullivan G.M., McEwen B.S., Gorman J.M., and LeDoux J.E. The selective serotonin reuptake inhibitor citalopram increases fear after acute treatment but reduces fear with chronic treatment. a comparison with tianeptine. Biol Psychiatry 55 (2004) 1171-1178
12. Carlsson M., Svensson K., Eriksson E., and Carlsson A. Rat brain serotonin. biochemical and functional evidence for a sex difference. J Neural Transm 63 (1985) 297-313
13. Clark J.A., Pai L.Y., Flick R.B., and Rohrer S.P. Differential hormonal regulation of tryptophan hydroxylase-2 mRNA in the murine dorsal raphe nucleus. Biol Psychiatry 57 (2005) 943-946
14. Clark MS, McDevitt RA, Neumaier JF (in press): Quantitative mapping of tryptophan hydroxylase-2, 5-HT1A, 5-HT1B, and serotonin transporter expression across the anteroposterior axis of the rat dorsal and median raphe nuclei. J Comp Neurol.
15. Diaz-Veliz G., Urresta F., Dussaubat N., and Mora S. Progesterone effects on the acquisition of conditioned avoidance responses an other motoric behaviors in intact and ovariectomized rats. Psychoneuroendocrinology 19 (1994) 387-394
16. Durand M., Berton O., Aguerre S., Edno L., Combourieu I., Mormede P., et al. Effects of repeated fluoxetine on anxiety-related behaviours, central serotonergic systems, and the corticotropic axis axis in SHR and WKY rats. Neuropharmacology 38 (1999) 893-907
17. Freeman M.E. The Neuroendocrine Control of the Ovarian Cycle of the Rat. In: Knobil E., and Neill J.D. (Eds). The Physiology of Reproduction. Second ed. (1994), Raven Press, Ltd, New York 613-648
18. Gregoire A.J., Kumar R., Everitt B., Henderson A.F., and Studd J.W. Transdermal oestrogen for treatment of severe postnatal depression. Lancet 347 (1996) 930-933
19. Griebel G. 5-Hydroxytryptamine-interacting drugs in animal models of anxiety disorders. more than 30 years of research. Pharmacol Ther 65 (1995) 319-395
20. Gundlah C., Alves S.E., Clark J.A., Pai L.Y., Schaeffer J.M., and Rohrer S.P. Estrogen receptor-beta regulates tryptophan hydroxylase-1 expression in the murine midbrain raphe. Biol Psychiatry 57 (2005) 938-942
21. Halbreich U., Rojansky N., Palter S., Tworek H., Hissin P., and Wang K. Estrogen augments serotonergic activity in postmenopausal women. Biol Psychiatry 37 (1995) 434-441
22. Haleem D.J., Kennett G.A., and Curzon G. Hippocampal 5-hydroxytryptamine synthesis is greater in female rats than in males and more decreased by the 5-HT1A agonist 8-OH-DPAT. J Neural Transm Gen Sect 79 (1990) 93-101
23. Hammack S.E., Richey K.J., Schmid M.J., LoPresti M.L., Watkins L.R., and Maier S.F. The role of corticotropin-releasing hormone in the dorsal raphe nucleus in mediating the behavioral consequences of uncontrollable stress. J Neurosci 22 (2002) 1020-1026
24. Handley S.L., McBlane J.W., Critchley M.A., and Njung'e K. Multiple serotonin mechanisms in animal models of anxiety. environmental, emotional and cognitive factors. Behav Brain Res 58 (1993) 203-210
25. Herzog A.G. Psychoneuroendocrine aspects of temporolimbic epilepsy. Part I. Brain, reproductive steroids, and emotions. Psychosomatics 40 (1999) 95-101
26. Hiroi R., and Neumaier J.F. Differential effects of ovarian steroids on anxiety versus fear as measured by open field test and fear-potentiated startle. Behavioural Brain Research 166 (2006) 93-100
27. Hope W.G., Bruns M.E., and Thomas M.L. Regulation of duodenal insulin-like growth factor I and active calcium transport by ovariectomy in female rats. Proc Soc Exp Biol Med 200 (1992) 528-535
28. Hoplight B.J., Vincow E.S., and Neumaier J.F. The effects of SB 224289 on anxiety and cocaine-related behaviors in a novel object task. Physiol Behav 84 (2005) 707-714
29. Izumi J., Washizuka M., Hayashi-Kuwabara Y., Yoshinaga K., Tanaka Y., Ikeda Y., et al. Evidence for a depressive-like state induced by repeated saline injections in Fischer 344 rats. Pharmacol Biochem Behav 57 (1997) 883-888
30. Kirby L.G., Allen A.R., and Lucki I. Regional differences in the effects of forced swimming on extracellular levels of 5-hydroxytryptamine and 5-hydroxyindoleacetic acid. Brain Res 682 (1995) 189-196
31. Kirby L.G., Chou-Green J.M., Davis K., and Lucki I. The effects of different stressors on extracellular 5-hydroxytryptamine and 5-hydroxyindoleacetic acid. Brain Res 760 (1997) 218-230
32. Kirby L.G., Rice K.C., and Valentino R.J. Effects of corticotropin-releasing factor on neuronal activity in the serotonergic dorsal raphe nucleus. Neuropsychopharmacology 22 (2000) 148-162
33. Koss W.A., Gehlert D.R., and Shekhar A. Different effects of subchronic doses of 17-beta estradiol in two ethologically based models of anxiety utilizing female rats. Horm Behav 46 (2004) 158-164
34. Lindberg M.K., Moverare S., Skrtic S., Gao H., Dahlman-Wright K., Gustafsson J.A., et al. Estrogen receptor (ER)-beta reduces ERalpha-regulated gene transcription, supporting a "ying yang" relationship between ERalpha and ERbeta in mice. Mol Endocrinol 17 (2003) 203-208
35. Liu M.M., Albanese C., Anderson C.M., Hilty K., Webb P., Uht R.M., et al. Opposing action of estrogen receptors alpha and beta on cyclin D1 gene expression. J Biol Chem 277 (2002) 24353-24360
36. Lowry C.A. Functional subsets of serotonergic neurones. implications for control of the hypothalamic-pituitary-adrenal axis. J Neuroendocrinol 14 (2002) 911-923
37. Lu H., Ozawa H., Nishi M., Ito T., and Kawata M. Serotonergic neurones in the dorsal raphe nucleus that project into the medial preoptic area contain oestrogen receptor beta. J Neuroendocrinol 13 (2001) 839-845
38. Lu N.Z., Shlaes T.A., Gundlah C., Dziennis S.E., Lyle R.E., and Bethea C.L. Ovarian steroid action on tryptophan hydroxylase protein and serotonin compared to localization of ovarian steroid receptors in midbrain of guinea pigs. Endocrine 11 (1999) 257-267
39. Lund B.C., Bever-Stille K.A., and Perry P.J. Testosterone and andropause. the feasibility of testosterone replacement therapy in elderly men. Pharmacotherapy 19 (1999) 951-956
40. Lund T.D., Rovis T., Chung W.C., and Handa R.J. Novel actions of estrogen receptor-beta on anxiety-related behaviors. Endocrinology 146 (2005) 797-807
41. Maes M., and Meltzer H.Y. The serotonin hypothesis of major depression. In: Bloom F.E., and Kupfer D.J. (Eds). Psychopharmacology. The Fourth Generation of Progress (1995), Raven Press, New York 933-944
42. Matthews J., and Gustafsson J.A. Estrogen signaling. a subtle balance between ER alpha and ER beta. Mol Interv 3 (2003) 281-292
43. McQueen J.K., Wilson H., and Fink G. Estradiol-17 beta increases serotonin transporter (SERT) mRNA levels and the density of SERT-binding sites in female rat brain. Brain Res Mol Brain Res 45 (1997) 13-23
44. Molliver M.E. Serotonergic neuronal systems. what their anatomic organization tells us about function. J Clin Psychopharmacol 7 (1987) 3S-23S
45. Morgan M.A., Schulkin J., and Pfaff D.W. Estrogens and nonreproductive behaviors related to activity and fear. Neurosci Biobehav Rev 28 (2004) 55-63
46. Nash M.W., Sugden K., Huezo-Diaz P., Williamson R., Sterne A., Purcell S., et al. Association analysis of monoamine genes with measures of depression and anxiety in a selected community sample of siblings. Am J Med Genet B Neuropsychiatr Genet 135 (2005) 33-37
47. Palanza P. Animal models of anxiety and depression. how are females different?. Neurosci Biobehav Rev 25 (2001) 219-233
48. Pare W.P. Open field, learned helplessness, conditioned defensive burying, and forced-swim tests in WKY rats. Physiol Behav 55 (1994) 433-439
49. Paxinos G., and Watson C. The rat brain in stereotaxic coordinates. second ed. (1986), Academic Press, Inc, San Diego
50. Pecins-Thompson M., Brown N.A., Kohama S.G., and Bethea C.L. Ovarian steroid regulation of tryptophan hydroxylase mRNA expression in rhesus macaques. J Neurosci 16 (1996) 7021-7029
51. Peyron C., Petit J.M., Rampon C., Jouvet M., and Luppi P.H. Forebrain afferents to the rat dorsal raphe nucleus demonstrated by retrograde and anterograde tracing methods. Neuroscience 82 (1998) 443-468
52. Pigott T.A. Anxiety disorders in women. Psychiatr Clin North Am 26 (2003) 621-672 vi-vii
53. Price M.L., Curtis A.L., Kirby L.G., Valentino R.J., and Lucki I. Effects of corticotropin-releasing factor on brain serotonergic activity. Neuropsychopharmacology 18 (1998) 492-502
54. Prut L., and Belzung C. The open field as a paradigm to measure the effects of drugs on anxiety-like behaviors. a review. Eur J Pharmacol 463 (2003) 3-33
55. Ramos A., Berton O., Mormede P., and Chaouloff F. A multiple-test study of anxiety-related behaviours in six inbred rat strains. Behav Brain Res 85 (1997) 57-69
56. Robichaud M., and Debonnel G. Oestrogen and testosterone modulate the firing activity of dorsal raphe nucleus serotonergic neurones in both male and female rats. J Neuroendocrinol 17 (2005) 179-185
57. Roche M., Commons K.G., Peoples A., and Valentino R.J. Circuitry underlying regulation of the serotonergic system by swim stress. J Neurosci 23 (2003) 970-977
58. Rosecrans J.A. Differences in brain area 5-hydroxytryptamine turnover and rearing behavior in rats and mice of both sexes. Eur J Pharmacol 9 (1970) 379-382
59. Rubinow D.R. Reproductive steroids in context. Arch Women Ment Health 8 (2005) 1-5
60. Rubinow D.R., Schmidt P.J., and Roca C.A. Estrogen-serotonin interactions. implications for affective regulation. Biol Psychiatry 44 (1998) 839-850
61. Sanchez R.L., Reddy A.P., Centeno M.L., Henderson J.A., and Bethea C.L. A second tryptophan hydroxylase isoform, TPH-2 mRNA, is increased by ovarian steroids in the raphe region of macaques. Brain Res Mol Brain Res 135 (2005) 194-203
62. Sandford J.J., Argyropoulos S.V., and Nutt D.J. The psychobiology of anxiolytic drugs. Part 1: Basic neurobiology. Pharmacol Ther 88 (2000) 197-212
63. Schmidt P.J., Nieman L.K., Danaceau M.A., Adams L.F., and Rubinow D.R. Differential behavioral effects of gonadal steroids in women with and in those without premenstrual syndrome. N Engl J Med 338 (1998) 209-216
64. Sell S.L., Scalzitti J.M., Thomas M.L., and Cunningham K.A. Influence of ovarian hormones and estrous cycle on the behavioral response to cocaine in female rats. J Pharmacol Exp Ther 293 (2000) 879-886
65. Shughrue P.J., Lane M.V., and Merchenthaler I. Comparative distribution of estrogen receptor-alpha and -beta mRNA in the rat central nervous system. J Comp Neurol 388 (1997) 507-525
66. Sichel D.A., Cohen L.S., Robertson L.M., Ruttenberg A., and Rosenbaum J.F. Prophylactic estrogen in recurrent postpartum affective disorder. Biol Psychiatry 38 (1995) 814-818
67. Smith E.R., Damassa D.A., and Davidson J.M. Hormone administration. peripheral and intracranial implants. In: Meyer R.D. (Ed). Methods of Psychobiology (1978), Academy, New York 259-279
68. Smith M.S., Freeman M.E., and Neill J.D. The control of progesterone secretion during the estrous cycle and early pseudopregnancy in the rat. prolactin, gonadotropin and steroid levels associated with rescue of the corpus luteum of pseudopregnancy. Endocrinology 96 (1975) 219-226
69. Steiner M., Dunn E., and Born L. Hormones and mood. from menarche to menopause and beyond. J Affect Disord 74 (2003) 67-83
70. Sumner B.E., Grant K.E., Rosie R., Hegele-Hartung C., Fritzemeier K.H., and Fink G. Effects of tamoxifen on serotonin transporter and 5-hydroxytryptamine(2A) receptor binding sites and mRNA levels in the brain of ovariectomized rats with or without acute estradiol replacement. Brain Res Mol Brain Res 73 (1999) 119-128
71. Sun H.S., Tsai H.W., Ko H.C., Chang F.M., and Yeh T.L. Association of tryptophan hydroxylase gene polymorphism with depression, anxiety and comorbid depression and anxiety in a population-based sample of postpartum Taiwanese women. Genes Brain Behav 3 (2004) 328-336
72. Thomas E., Pernar L., Lucki I., and Valentino R.J. Corticotropin-releasing factor in the dorsal raphe nucleus regulates activity of lateral septal neurons. Brain Res 960 (2003) 201-208
73. Vaccari A., Brotman S., Cimino J., and Timiras P.S. Sex differentiation of neurotransmitter enzymes in central and peripheral nervous systems. Brain Res 132 (1977) 176-185
74. Vertes R.P. A PHA-L analysis of ascending projections of the dorsal raphe nucleus in the rat. J Comp Neurol 313 (1991) 643-668
75. Vertes R.P., Fortin W.J., and Crane A.M. Projections of the median raphe nucleus in the rat. J Comp Neurol 407 (1999) 555-582
76. Walther D.J., and Bader M. A unique central tryptophan hydroxylase isoform. Biochem Pharmacol 66 (2003) 1673-1680
77. You J.S., Hu S.Y., Chen B., and Zhang H.G. Serotonin transporter and tryptophan hydroxylase gene polymorphisms in Chinese patients with generalized anxiety disorder. Psychiatr Genet 15 (2005) 7-11
78. Zhang X., Gainetdinov R.R., Beaulieu J.M., Sotnikova T.D., Burch L.H., Williams R.B., et al. Loss-of-function mutation in tryptophan hydroxylase-2 identified in unipolar major depression. Neuron 45 (2005) 11-16
79. Zhou W., Cunningham K.A., and Thomas M.L. Estrogen regulation of gene expression in the brain. a possible mechanism altering the response to psychostimulants in female rats. Brain Res Mol Brain Res 100 (2002) 75-83
80. Zill P., Baghai T.C., Zwanzger P., Schule C., Eser D., Rupprecht R., et al. SNP and haplotype analysis of a novel tryptophan hydroxylase isoform (TPH2) gene provide evidence for association with major depression. Mol Psychiatry 9 (2004) 1030-1036